scholarly journals Estimating maximal microbial growth rates from cultures, metagenomes, and single cells via codon usage patterns

2021 ◽  
Vol 118 (12) ◽  
pp. e2016810118
Author(s):  
Jake L. Weissman ◽  
Shengwei Hou ◽  
Jed A. Fuhrman

Maximal growth rate is a basic parameter of microbial lifestyle that varies over several orders of magnitude, with doubling times ranging from a matter of minutes to multiple days. Growth rates are typically measured using laboratory culture experiments. Yet, we lack sufficient understanding of the physiology of most microbes to design appropriate culture conditions for them, severely limiting our ability to assess the global diversity of microbial growth rates. Genomic estimators of maximal growth rate provide a practical solution to survey the distribution of microbial growth potential, regardless of cultivation status. We developed an improved maximal growth rate estimator and predicted maximal growth rates from over 200,000 genomes, metagenome-assembled genomes, and single-cell amplified genomes to survey growth potential across the range of prokaryotic diversity; extensions allow estimates from 16S rRNA sequences alone as well as weighted community estimates from metagenomes. We compared the growth rates of cultivated and uncultivated organisms to illustrate how culture collections are strongly biased toward organisms capable of rapid growth. Finally, we found that organisms naturally group into two growth classes and observed a bias in growth predictions for extremely slow-growing organisms. These observations ultimately led us to suggest evolutionary definitions of oligotrophy and copiotrophy based on the selective regime an organism occupies. We found that these growth classes are associated with distinct selective regimes and genomic functional potentials.

2020 ◽  
Author(s):  
Jake L. Weissman ◽  
Shengwei Hou ◽  
Jed A. Fuhrman

AbstractMaximal growth rate is a basic parameter of microbial lifestyle that varies over several orders of magnitude, with doubling times ranging from a matter of minutes to multiple days. Growth rates are typically measured using laboratory culture experiments. Yet, we lack sufficient understanding of the physiology of most microbes to design appropriate culture conditions for them, severely limiting our ability to assess the global diversity of microbial growth rates. Genomic estimators of maximal growth rate provide a practical solution to survey the distribution of microbial growth potential, regardless of cultivation status. We developed an improved maximal growth rate estimator, and implement this estimator in an easy-to-use R package (gRodon), which outperforms the state-of-the-art growth estimator in multiple settings, including in a community context where we implement a novel species abundance correction for metagenomes. Additionally, we estimate maximal growth rates from over 200,000 genomes, metagenome-assembled genomes, and single-cell amplified genomes to survey growth potential across the range of prokaryotic diversity. We provide these compiled maximal growth rates in a publicly-available database (EGGO), which we use to illustrate how culture collections show a strong bias towards organisms capable of rapid growth. We demonstrate how this database can be used to propagate maximal growth rate predictions to organisms for which we lack genomic information, on the basis of 16S rRNA sequence alone. Finally, we observe a bias in growth predictions for extremely slow-growing organisms, ultimately leading us to suggest a novel evolutionary definition of oligotrophy based on the selective regime an organism occupies.SignificanceDespite the wide perception that microbes have rapid growth rates, many environments like seawater and soil are often dominated by microorganisms that can only grow very slowly. Our knowledge about growth is necessarily biased towards easily culturable organisms, which turn out to be those that tend to grow fast, because microbial growth rates have traditionally been measured using lab growth experiments. But how are potential growth rates distributed in nature? We developed a tool to predict maximum growth rate from an organism’s genome sequence (gRodon). We predicted the growth rates of over 200,000 organisms and compiled these predictions in a publicly-available database (EGGO), which illustrates how current collections of cultured microbes are strongly biased towards fast-growing organisms.


2021 ◽  
Author(s):  
Jake L Weissman ◽  
Edward-Robert O Dimbo ◽  
Arianna I Krinos ◽  
Christopher Neely ◽  
Yuniba Yagues ◽  
...  

Microbial eukaryotes are ubiquitous in the environment and play important roles in key ecosystem processes, including accounting for a significant portion of global primary production. Yet, our tools for assessing the functional capabilities of eukaryotic microbes in the environment are quite limited because many microbes have yet to be grown in culture. Maximum growth rate is a fundamental parameter of microbial lifestyle that reveals important information about an organism's functional role in a community. We developed and validated a genomic estimator of maximum growth rate for eukaryotic microbes, enabling the assessment of growth potential for both cultivated and yet-to-be-cultivated organisms. We produced a database of over 700 growth predictions from genomes, transcriptomes, and metagenome-assembled genomes, and found that closely related and/or functionally similar organisms tended to have similar maximal growth rates. By comparing the maximal growth rates of existing culture collections with environmentally-derived genomes we found that, unlike for prokaryotes, culture collections of microbial eukaryotes are only minimally biased in terms of growth potential. We then extended our tool to make community-wide estimates of growth potential from over 500 marine metagenomes, mapping growth potential across the global oceans. We found that prokaryotic and eukaryotic communities have highly correlated growth potentials near the ocean surface, but that this relationship disappears deeper in the water column. This suggests that fast growing eukaryotes and prokaryotes thrive under similar conditions at the ocean surface, but that there is a decoupling of these communities as resources become scarce deeper in the water column.


1984 ◽  
Vol 17 (1) ◽  
pp. 45-82 ◽  
Author(s):  
Måns Ehrenberg ◽  
C. G. Kurland

The present study is best understood as an extension and critique of two schools of thought. The first is that of Malloe and his students, among whom we number ourselves. It is to Maaloe that we are indebted for the idea that logarithmically growing bacteria assemble and use tibosomes in amounts that are optimally adjusted to yield the maximal growth rates supported by different media. Her, we begin our analysis by applying this optimization priciple to all the components of a logarithmically growing system. Our objective is to use the growth optimization constraint as a tool to explore the physiological limits on the accuracy of gene expression. This brings us to our second source of inspiration, which is Orgel's (1963) conception of a problem that Ninio (1982) has referred to as the ‘great error loop’.


2003 ◽  
Vol 69 (9) ◽  
pp. 5685-5689 ◽  
Author(s):  
Joseph O. Falkinham

ABSTRACT The susceptibility of representative strains of Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum (the MAIS group) to chlorine was studied to identify factors related to culture conditions and growth phase that influenced susceptibility. M. avium and M. intracellulare strains were more resistant to chlorine than were strains of M. scrofulaceum. Transparent and unpigmented colony variants were more resistant to chlorine than were their isogenic opaque and pigmented variants (respectively). Depending on growth stage and growth rate, MAIS strains differed in their chlorine susceptibilities. Cells from strains of all three species growing in early log phase at the highest growth rates were more susceptible than cells in log and stationary phase. Rapidly growing cells were more susceptible to chlorine than slowly growing cells. The chlorine susceptibility of M. avium cells grown at 30°C was increased when cells were exposed to chlorine at 40°C compared to susceptibility after exposure at 30°C. Cells of M. avium grown in 6% oxygen were significantly more chlorine susceptible than cells grown in air. Chlorine-resistant MAIS strains were more hydrophobic and resistant to Tween 80, para-nitrobenzoate, hydroxylamine, and nitrite than were the chlorine-sensitive strains.


1999 ◽  
Vol 65 (6) ◽  
pp. 2631-2635 ◽  
Author(s):  
Sonja Isken ◽  
Antoine Derks ◽  
Petra F. G. Wolffs ◽  
Jan A. M. de Bont

ABSTRACT Solvent-tolerant microorganisms are useful in biotransformations with whole cells in two-phase solvent-water systems. The results presented here describe the effects that organic solvents have on the growth of these organisms. The maximal growth rate of Pseudomonas putida S12, 0.8 h−1, was not affected by toluene in batch cultures, but in chemostat cultures the solvent decreased the maximal growth rate by nearly 50%. Toluene, ethylbenzene, propylbenzene, xylene, hexane, and cyclohexane reduced the biomass yield, and this effect depended on the concentration of the solvent in the bacterial membrane and not on its chemical structure. The dose response to solvents in terms of yield was linear up to an approximately 200 mM concentration of solvent in the bacterial membrane, both in the wild type and in a mutant lacking an active efflux system for toluene. Above this critical concentration the yield of the wild type remained constant at 0.2 g of protein/g of glucose with increasing concentrations of toluene. The reduction of the yield in the presence of solvents is due to a maintenance higher by a factor of three or four as well as to a decrease of the maximum growth yield by 33%. Therefore, energy-consuming adaptation processes as well as the uncoupling effect of the solvents reduce the yield of the tolerant cells.


1984 ◽  
Vol 103 (1) ◽  
pp. 137-153 ◽  
Author(s):  
J. E. Frisch ◽  
T. E. Vercoe

SummaryCalves from three breeds, Brahman, Hereford × Shorthorn (HS) and Brahman × HS (BX), were divided equally into two groups, one of which was treated every 3 weeks from birth onwards to control ticks and gastrointestinal helminths, and one of which was untreated. Mortalities, growth rates and levels of resistance to environmental stresses that affected both mortality and growth under grazing conditions were recorded for all animals up to weaning (6 months) and for all males up to 15 months of age. The Brahmans were the most and the HS were the least resistant to environmental stresses, each of which was shown to depress growth in proportion to its magnitude and to contribute to the high mortalities of the HS. All breeds responded positively to parasite control with the greatest response in both survival and growth in the HS breed and the least response in the Brahman breed.Samples of males from the various breed-treatment groups were taken into pens where they were protected from environmental stresses and fed both low-quality pasture hay and high-quality lucerne hay ad libitum. Measurements were made of fasting metabolism, maintenance requirement, voluntary food intake and gain, variables related to the growth potential of each animal. The HS animals had the highest whilst the Brahmans had the lowest values for each variable.However, despite their low growth potential, the Brahmans had the highest growtli rate, and the HS, despite their high growth potential, had the lowest growth rate, when growth was measured in the presence of all environmental stresses. When parasites were controlled, growth rates were highest for the BX, the breed with intermediate growtli potential, and did not differ between the HS and Brahmans. These interactions arose because of the different contributions of resistance to environmental stresses and growth potential to growth rate measured at the different levels of environmental stresses. The relevance of these interactions to breed evaluation and cross-breeding is considered.Growth potential and resistance to environmental stresses were negatively correlated both between and within breeds, though the latter was biased by the effects of compensation. The influence of these relationships on the likely outcome of selection for increased growth rate, both between and within breeds, is discussed.


2008 ◽  
Vol 30 (6) ◽  
pp. 419-424 ◽  
Author(s):  
Jun Ah Lee ◽  
Min Suk Kim ◽  
Dong Ho Kim ◽  
Jung Sub Lim ◽  
Kyung Duk Park ◽  
...  

2017 ◽  
Vol 60 (4) ◽  
pp. 427-437 ◽  
Author(s):  
Philipp C. Muth ◽  
Anne Valle Zárate

Abstract. The effects of the increase of body weight of contemporary broilers during growth on functional meat quality and color characteristics of the chicken breast muscle are controversially debated. Therefore, male chickens (n = 264) of a fast-growing commercial broiler (Ross 308) and two slow-growing experimental meat-type chicken lines were compared at equal age and at similar body weight in order to investigate the effect of growth rate on selected functional breast meat traits and meat color. Additionally, the breast meat characteristics of birds with different growth profiles were compared within lines. When the body weight of commercial broilers reached about 40 to 60 % of their growth potential, they exhibited particularly high ultimate pH values compared with slow-growing lines. The ability of the meat of fast-growing broilers to retain water during cooking was impaired (5 to 16 percentage points increased cooking loss compared to slow-growing lines), which, in contrast to pH, was only marginally affected by body weight and/or age at slaughter. No unfavorable correlations of breast meat quality traits with the growth profile, represented by growth curve parameters derived from the Gompertz–Laird equation, were detected within any of the investigated chicken lines. It is noteworthy that the associations of ultimate pH and cooking loss with maximum growth speed indicate a non-linear relationship. Thus, some of the functional characteristics of breast meat of the fast-growing broiler resembled the white-striping defect described for poultry meat, but the hypothesis that selection on increased growth rates is detrimental for meat quality per se could not be confirmed. In fact, an elevated growth potential in particular, i.e., body weight at maturity, could have some beneficial effects for the water-holding capacity of breast meat, regardless of the genotypic growth rate.


2020 ◽  
Vol 10 (10) ◽  
pp. 3831-3842
Author(s):  
Christopher Kozela ◽  
Mark O. Johnston

Mutations shape genetic architecture and thus influence the evolvability, adaptation and diversification of populations. Mutations may have different and even opposite effects on separate fitness components, and their rate of origin, distribution of effects and variance-covariance structure may depend on environmental quality. We performed an approximately 1,500-generation mutation-accumulation (MA) study in diploids of the yeast Saccharomyces cerevisiae in stressful (high-salt) and normal environments (50 lines each) to investigate the rate of input of mutational variation (Vm) as well as the mutation rate and distribution of effects on diploid and haploid fitness components, assayed in the normal environment. All four fitness components in both MA treatments exhibited statistically significant mutational variance and mutational heritability. Compared to normal-MA, salt stress increased the mutational variance in growth rate by more than sevenfold in haploids derived from the MA lines. This increase was not detected in diploid growth rate, suggesting masking of mutations in the heterozygous state. The genetic architecture arising from mutation (M-matrix) differed between normal and salt conditions. Salt stress also increased environmental variance in three fitness components, consistent with a reduction in canalization. Maximum-likelihood analysis indicated that stress increased the genomic mutation rate by approximately twofold for maximal growth rate and sporulation rate in diploids and for viability in haploids, and by tenfold for maximal growth rate in haploids, but large confidence intervals precluded distinguishing these values between MA environments. We discuss correlations between fitness components in diploids and haploids and compare the correlations between the two MA environmental treatments.


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